Enzymatic antioxidant defences are transcriptionally regulated in Es524, a copper-tolerant strain of Ectocarpus siliculosus (Ectocarpales, Phaeophyceae)

REFERENCES

• Alaoui-Sossé B., Genet P., Vinit-Dunand F., Toussaint M.-L., Epron D. & Badot P.-M. 2004. Effect of copper on growth in cucumber plants (Cucumis sativus) and its relationships with carbohydrate accumulation and changes in ion contents. Plant Science 166: 1213–1218.
   Web of Science ®Google Scholar
• Bakthavatchalu V., Dey S., Xu Y., Noel T., Jungsuwadee P., Holley A.K., Dhar S.K., Batinic-Haberle I. & St Clair D.K. 2012. Manganese superoxide dismutase is a mitochondrial fidelity protein that protects Polgamma against UV-induced inactivation. Oncogene 31: 2129–2139.
   PubMed Web of Science ®Google Scholar
• Burkhead J.L., Gogolin Reynolds K.A., Abdel-Ghany S.E., Cohu C.M. & Pilon M. 2009. Copper homeostasis. New Phytologist 182: 799–816.
   PubMed Web of Science ®Google Scholar
• Chiappetta A., Greco M. & Bitonti M.B. 2006. Cytophysiological features of embryos in Posidonia oceanica seeds. Biologia Marina Mediterranea 39: 39–45.
   Google Scholar
• Chung I.K. & Brinkhuis B.H. 1986. Copper effects in early stages of the kelp, Laminaria saccharina. Marine Pollution Bulletin 17: 213–218.
   Web of Science ®Google Scholar
• Correa J.A., Castilla J.C., Ramirez M., Varas M., Lagos N., Vergara S., Moenne A., Roman D. & Brown M.T. 1999. Copper, copper mine tailings and their effect on marine algae in northern Chile. Journal of Applied Phycology 11: 57–67.
   Web of Science ®Google Scholar
• Gledhill M., Nimmo M., Hill S. & Brown M.T. 1999. The release of copper-complexing ligands by the brown alga Fucus vesiculosus (Phaeophyceae) in response to increasing total copper levels. Journal of Phycology 35: 501–509.
   Web of Science ®Google Scholar
• Greco M., Sáez C.A., Brown M.T. & Bitonti M.B. 2014. A simple and effective method for high quality co-extraction of genomic DNA and total RNA from low biomass Ectocarpus siliculosus, the model brown alga. PLoS ONE 9: e101190.
   Web of Science ®Google Scholar
• Heumann H.G. 1987. Effects of heavy metals on growth and ultrastructure of Chara vulgaris. Protoplasma 136: 37–48.
   Web of Science ®Google Scholar
• IBM. 2012. SPSS 21. http://www-01.ibm.com/software/analytics/spss/. IBM, New York, New York USA.
   Google Scholar
• Kuo W.Y., Huang C.H., Liu A.C., Cheng C.P., Li S.H., Chang W.C., Weiss C., Azem A. & Jinn T.L. 2013. CHAPERONIN 20 mediates iron superoxide dismutase (FeSOD) activity independent of its co-chaperonin role in Arabidopsis chloroplasts. New Phytologist 197: 99–110.
   PubMed Web of Science ®Google Scholar
• Le Bail A., Dittami S.M., de Franco P.O., Rousvoal S., Cock M.J., Tonon T. & Charrier B. 2008. Normalisation genes for expression analyses in the brown alga model Ectocarpus siliculosus. BMC Molecular Biology 9: 75.
   PubMed Web of Science ®Google Scholar
• Lee M.R. & Correa J.A. 2005. Effects of copper mine tailings disposal on littoral meiofaunal assemblages in the Atacama region of northern Chile. Marine Environmental Research 59: 1–18.
   PubMed Web of Science ®Google Scholar
• Mason M.G., Nicholls P., Wilson M.T. & Cooper C.E. 2006. Nitric oxide inhibition of respiration involves both competitive (heme) and noncompetitive (copper) binding to cytochrome c oxidase. Proceedings of the National Academy of Sciences of the United States of America 103: 708–713.
   PubMed Web of Science ®Google Scholar
• Mellado M., Contreras R.A., González A., Dennett G. & Moenne A. 2012. Copper-induced synthesis of ascorbate, glutathione and phytochelatins in the marine alga Ulva compressa (Chlorophyta). Plant Physiology and Biochemistry 51: 102–108.
   PubMed Web of Science ®Google Scholar
• Morel F.M.M., Rueter J.G., Anderson D.M. & Guillard R.R.L. 1979. Aquil: a chemically defined phytoplankton culture medium for trace metal studies. Journal of Phycology 15: 135–141.
   Web of Science ®Google Scholar
• National Institutes of Health. 2011. Image J, version 1.45k. Website title, National Institutes of Health, Washington, D.C. USA.
   Google Scholar
• Nielsen H.D., Brown M.T. & Brownlee C. 2003a. Cellular responses of developing Fucus serratus embryos exposed to elevated concentrations of Cu2+. Plant Cell & Environment 26: 1737–1747.
   Web of Science ®Google Scholar
• Nielsen H.D., Brownlee C., Coelho S.M. & Brown M.T. 2003b. Inter-population differences in inherited copper tolerance involve photosynthetic adaptation and exclusion mechanisms in Fucus serratus. New Phytologist 160: 157–165.
   PubMed Web of Science ®Google Scholar
• Ortega K.J., Sáez C.A. & Macaya E.C. 2014. Changes in invertebrate assemblages inhabiting Lessonia spicata (Phaeophyceae) holdfasts after the 2010 earthquake-mediated coastal uplift in Chile. Revista de Biología Marina y Oceanografía 49: 129–134.
   Web of Science ®Google Scholar
• Ouzounidou G., Čiamporová M., Moustakas M. & Karataglis S. 1995. Responses of maize (Zea mays L.) plants to copper stress – growth, mineral content and ultrastructure of roots. Environmental and Experimental Botany 35: 167–176.
   Web of Science ®Google Scholar
• Percival E. & McDowell R.H. 1981. Algal cell walls, composition and biosynthesis. Encyclopedia of Plant Physiology 13B: 277–316.
   Google Scholar
• Pinto E., Sigaud-Kutner T.C.S., Leitao M.A.S., Okamoto O.K., Morse D. & Colepicolo P. 2003. Heavy metal-induced oxidative stress in algae. Journal of Phycology 39: 1008–1018.
   Web of Science ®Google Scholar
• Riisgård H.U. 1979. Effect of copper on volume regulation in the marine flagellate Dunaliella marina. Marine Biology 50: 189–193.
   Web of Science ®Google Scholar
• Ritter A., Dittami S.M., Goulitquer S., Correa J.A., Boyen C., Potin P. & Tonon T. 2014. Transcriptomic and metabolomic analysis of copper stress acclimation in Ectocarpus siliculosus highlights signaling and tolerance mechanisms in brown algae. BMC Plant Biology 14: 116.
   Web of Science ®Google Scholar
• Roncarati F., Sáez C.A., Greco M., Gledhill M., Bitonti M.B. & Brown M.T. 2015. Response differences between Ectocarpus siliculosus populations to copper stress involve cellular exclusion and induction of the phytochelatin biosynthetic pathway. Aquatic Toxicology 159: 167–175.
   Web of Science ®Google Scholar
• Sáez C.A., Lobos M.G., Macaya E., Oliva D., Quiroz W. & Brown M.T. 2012a. Variation in patterns of metal accumulation in thallus parts of Lessonia trabeculata (Laminariales; Phaeophyceae): implications for biomonitoring. PLoS ONE 7: e50170.
   Web of Science ®Google Scholar
• Sáez C.A., Pérez-Matus A., Lobos M.G., Oliva D., Vásquez J.A. & Bravo M. 2012b. Environmental assessment in a shallow subtidal rocky habitat: approach coupling chemical and ecological tools. Chemistry and Ecology 28: 1–15.
   Web of Science ®Google Scholar
• Sáez C.A., González A., Contreras R., Moody J., Moenne A. & Brown M.T. 2015a. A novel field transplantation technique reveals intra-specific metal-induced oxidative responses in strains of Ectocarpus siliculosus with different pollution histories. Environmental Pollution 199: 130–138.
   Web of Science ®Google Scholar
• Sáez C.A., Roncarati F., Moenne A., Moody J.A. & Brown M.T. 2015b. Copper-induced intra-specific oxidative damage and antioxidant responses in strains of the brown alga Ectocarpus siliculosus with different pollution histories. Aquatic Toxicology 159: 81–89.
   Web of Science ®Google Scholar
• Smith S.D.A. 1996. The macrofaunal community of Ecklonia radiata holdfasts: variation associated with sediment regime, sponge cover and depth. Australian Journal of Ecology 21: 144–153.
   Web of Science ®Google Scholar
• Sorbo S., Sinkkonen A., Aprile G., Strumia S., Cobianchi R.C., Leone A. & Basile A. 2011. Ultrastructural effects of trace elements and environmental pollution in Italian ‘Triangle of Death’ on Pseudevernia furfuracea (L.) Zopf. Plant Biosystems – An International Journal Dealing with All Aspects of Plant Biology 145: 461–471.
   Web of Science ®Google Scholar
• Tarakhovskaya E.R., Bilova T.E. & Maslov Y.I. 2015. Hydrogen peroxide content and vanadium-dependent haloperoxidase activity in thalli of six species of Fucales (Phaeophyceae). Phycologia 54: 417–424.
   Web of Science ®Google Scholar
• Tarhanen S. 1998. Ultrastructural responses of the lichen Bryoria fuscescensto simulated acid rain and heavy metal deposition. Annals of Botany 82: 735–746.
   Web of Science ®Google Scholar
• Visviki I. & Rachlin J.W. 1994. Acute and chronic exposure of Dunaliella salina and Chlamydomonas bullosa to copper and cadmium: effects of ultrastructure. Archives of Environmental Contamination and Toxicology 26: 154–162.
   PubMed Web of Science ®Google Scholar
• Wainwright S.J. & Woolhouse H.W. 1977. Some physiological aspects of copper and zinc tolerance in Agrostis tenuis Sibth.: cell elongation and membrane damage. Journal of Experimental Botany 28: 1029–1036.
   Web of Science ®Google Scholar
• Zhang X.-L., Jia X.-F., Yu B., Gao Y. & Bai J.-G. 2011. Exogenous hydrogen peroxide influences antioxidant enzyme activity and lipid peroxidation in cucumber leaves at low light. Scientia Horticulturae 129: 656–662.
   Web of Science ®Google Scholar